Archaea as Global Explorers: Let`s Exchange ATPase and Occupy More Extreme Habitats!

The membrane rotary energy-yielding ATPases represent the cornerstone of cellular bioenergetics for all three domains of life. The archaeal ATPases (A-type ATPases) are functionally similar to the eukaryotic and bacterial F-type ATPases that catalyze ATP synthesis using a PMF. However, they are structurally more similar to the vacuolar-type (V-type) ATPases of eukaryotes and some bacteria that function as proton pumps driven by ATP hydrolysis. Significant variation in subunit composition, structure, and mechanism of the archaeal ATPases is thought to confer adaptive advantage in the variety of extreme environments that archaea inhabit.

The ammonia-oxidizing archaea are recognized to exert primary control of nitrification in the marine environment, are major contributors to soil nitrification, and have a habitat range extending from geothermal systems, to acidic soils and the oceanic abyss. The basis for their remarkable adaptive radiation is obscured by a relatively simple metabolism – autotrophic growth using ammonia for energy and nitrogen. In this study, we find that their adaptation to acidic habitats and the extreme pressures of the hadal zone of the ocean at depths below 6000 meters is correlated with horizontal transfer of a variant of the energy-yielding ATPase (atp) operon. Whereas the ATPase genealogy of neutrophilic soil and upper ocean pelagic AOA is congruent with their organismal genealogy inferred from concatenated conserved proteins, a common clade of V-type ATPases unites phylogenetically disparate clades of acidophilic and piezophilic species.

A function of the so-acquired V-ATPases in pumping excessive cytoplasmic protons at low pH is consistent with its increased expression by acid-tolerant AOA with decreasing pH. Consistently, heterologous expression of the thaumarchaeotal V-ATPase significantly increased the growth rate of E.coli at low pH. Additional support for adaptive significance derives from our observation that horizontal transfer is also associated with the adaptive radiation of Micrarchaeota, Parvarchaeota and Marsarchaeota into acidic environments. Their ATPases are affiliated with the acidophilic lineage ATPases of Thermoplasmatales and phylogenetically divergent from the corresponding species tree.

Another notable finding is that single hadopelagic AOA species contain both A- and V-type ATPases, suggesting that extensive horizontal transfer of atp operons is a highly active and ongoing process within AOA. The presence of an additional V-type ATPase in hadopelagic AOA may provide fitness advantages in the deep ocean with elevated hydrostatic pressure, as the proposed function of V-ATPase in pumping excessive cytoplasmic protons at high pressure may serve to maintain the cytosolic pH homeostasis in marine AOA.

Taken together, our study provides the first clear evidence of a significant role of horizontal transfer of atp operon in the adaptive radiation of AOA, one of the most successful organisms on Earth, and other archaeal species, spanning the TACK and DPANN superphyla as well as Euryarchaeota phylum.